Feline Sino-orbital Fungal Infection Caused by Aspergillus and Scopulariopsis - seer ufrgs
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Acta Scientiae Veterinariae, 2019. 47(Suppl 1): 383. CASE REPORT ISSN 1679-9216 Pub. 383 Feline Sino-orbital Fungal Infection Caused by Aspergillus and Scopulariopsis Fernanda Vieira Amorim da Costa1, Andreia Spanamberg2, Ricardo Araujo3,4, Juliana Werner5 & Laerte Ferreiro2 ABSTRACT Background: Deep fungal infections of the orbit and nasal passages causing rhinitis and ulcerative keratomycosis are uncommonly reported in cats. Hyalohyphomycetes and phaeohyphomycetes have rarely been associated with this disorder. Sino-orbital fungal diseases are emerging and more invasive than sino-nasal fungal diseases with poor response to therapy and a worse prognosis. Brachycephalic feline breeds seem to be at increased risk for development of upper respiratory fungal diseases. Diagnosis is based on the demonstration of fungal hyphae by cytology or histology and definitive confir- mation by fungal culture and molecular methods. This is the first case report of a cat with clinical mixed fungal ball with Aspergillus and Scopulariopsis in Brazil. Case: A 3-year-old male Persian cat, in São José city, Santa Catarina, Brazil, was presented with exophthalmos and cor- neal ulcer of the left eye and protrusion, hyperemia, quemosis and fibroses of the left third eyelid. The retropulsion of the globe was negative in this eyeball and a presumptive diagnosis of a retrobulbar mass was made. The patient underwent a surgical procedure for inspection and collection of samples for bacterial and mycological culture. Culture revealed no bacterial growth, however, unique and abundant growth of Aspergillus spp. was present. A subconjunctival enucleation of the left eye was made and the mass was sent for histopathology examination. Histology showed inflammatory proliferative necrotizing pyogranulomatous reaction; with the presence of severe fungal infection evidenced by large number of hyaline septated regular and irregular mold hyphae. Molecular identification was performed using panfungal primers (ITS3-F / ITS4-R). Patient was treated with systemic itraconazole associated with amphotericin B and topical clotrimazole. A mass started to grow rapidly in the left pterygopalatine fossa and was surgically removed, but recurrence occurred seven days after. After 22 days of treatment, the animal died suddenly with a history of acute inspiratory dyspnea and cyanosis at the time prior to death. The diagnosis of sino-orbital fungal disease in the feline was based on clinical signs, mycological culture, histopathology and molecular methods. Discussion: Sino-orbital fungal diseases rare in cats and can result in significant injuries to the upper respiratory tract and eyes, sometimes resulting in enucleation and death. It seems feasible that a brachycephalic facial conformation may be an important risk factor for the development of sino-nasal fungal diseases in cats. Despite using selected drugs and eye enucleation to treat the disease, the cat developed a rapid growing oral mass that probably caused acute inspiratory dyspnea and death. Since no controlled studies exist on the treatment of feline fungal diseases, these cases are a challenge to the feline practitioner and this type of clinical manifestation should be included in the differential diagnosis of upper respiratory and ocular diseases. Keywords: Aspergilllus, cat, fungal disease, retrobulbar mass, upper respiratory disease. DOI: 10.22456/1679-9216.91581 Received: 8 December 2018 Accepted: 25 March 2019 Published: 10 April 2019 1 Setor de Medicina Felina do Hospital de Clínicas Veterinárias (HCV) & Setor de Micologia Veterinária, Faculdade de Veterinária (FaVet), Universidade 2 Federal do Rio Grande do Sul (UFRGS), Porto Alegre, RS, Brazil. 3i3S - Instituto de Investigação e Inovação em Saúde, Porto, Portugal. 4Department of Medical Biotechnology, College of Medicine and Public Health, Flinders University, Adelaide, South Australia, Australia. 5Werner & Werner - Labo- ratório de Patologia Veterinária, Curitiba, PR, Brazil. CORRESPONDENCE: F.V.A. Costa [fernanda.amorim@ufrgs.br - Tel.: +55 (51) 3308-9643]. Setor de Medicina Felina - HCV, UFRGS. Av. Bento Gonçalves n. 9090. Bairro Agronomia. CEP 91540-000 Porto Alegre, RS, Brazil. 1
F.V.A. Costa, A. Spanamberg, R. Araujo, J. Werner & L. Ferreiro. 2019. Feline Sino-orbital Fungal Infection Caused by Aspergillus and Scopulariopsis. Acta Scientiae Veterinariae. 47(Suppl 1): 383. INTRODUCTION However, the retropulsion of the globe was negative in Sino-nasal and sino-orbital fungal disease can be this eyeball. The left superior cornea had an irregular caused by hyalohyphomycetes (hyaline septate hyphae) form, corneal edema, neovascularization and retained and phaeohyphomycetes (pigmented septate hyphae). fluorescein stain (Fluoresceína Strips ®)4 [Figure 2]. Investigations suggested that the majority of infections A presumptive diagnosis of a retrobulbar mass was were caused by Aspergillus species. In cats, the disea- made. Furthermore, the cat had mucopurulent nasal se occurs in two main forms: sino-nasal aspergillosis and ocular discharge from the same side. (SNA) and sino-orbital aspergillosis (SOA) [5,16,29]. The patient had no fever or weight loss, but had SNA is characterized by signs of chronic nasal infection, a history of poor appetite and prostration. Immunoas- such as sneezing, uni or bilateral serous to mucopurulent says for the detection of feline immunodeficiency virus nasal discharge, and sometimes epistaxis. SOA is the and feline leukemia virus (FIV/FeLV) were negative. more invasive form because the fungus invades the sub- Complete blood count and serum biochemical assay mucosal tissue of the nasal cavity and sinus and extends were also performed, which showed only leukopenia through the orbital bone and into the retrobulbar space. and lymphopenia. Initial supportive therapy consisted SNO clinical signs include unilateral exophthalmos, of fluid and electrolyte therapy, eye drops of flurbipro- third eyelid prolapse, conjunctival hyperaemia and fen, moxifloxacin and chondroitin sulfate, in addition keratitis. Response to therapy is less successful in SNO to oral amoxicillin and cyproheptadine for 15 days. aspergillosis and the prognosis is generally worse [16]. After clinical improvement, the patient un- Definitive diagnosis requires a combination of derwent a surgical procedure for inspection and col- imaging, visualization of fungal plaques by rhinoscopy, lection of samples for cytology, culture, antimicrobial and identification of fungal structures on culture and sensitivity profile and histopathological analysis of cytology, or histopathology [4,29]. Treatment of this the mass. During the procedure, there was a purulent form of the disease should be multifactorial, including and caseous tissue in the third eyelid conjunctiva, oc- orbitotomy or eye enucleation and a combination of cupying the medial and retrobulbar region (Figure 3). systemic antifungal treatment with local therapy using Cytology showed the presence of red blood intranasal infusions under general anesthesia [16]. cells, predominance of degenerate neutrophils and few This is the first case report of a cat with cli- lymphocytes, and free and intracellular bacteria. Tissue nical mixed fungal infection with Aspergillus and fragments were subjected to aerobic culture at 37°C Scopulariopsis in Brazil showing details of the clinical on blood agar and MacConkey agar, and incubated at presentation, diagnosis, medical and surgical manage- 30°C on Sabouraud dextrose agar. Culture revealed ment of the disease. no bacterial growth, however, unique and abundant growth of Aspergillus spp. was present. CASE The patient was then submitted to radiographic A 3-year-old male Persian cat, weighing 3.8 kg investigation, which showed increased radiopacity in was seen at Green Cross Veterinary Clinic, São José, the left sinus and loss of definition of the turbinate Santa Catarina, Brazil, presenting with exophthalmos, bones. The cat underwent a surgical procedure for lagophthalmos and asymmetry of the frontal and dor- subconjunctival enucleation of the left eye (Figure sal face. Severe protrusion, hyperemia, chemosis and 4), which was sent for histopathology examination. fibrosis of the left third eyelid were noted (Figure 1). Histology showed inflammatory proliferative necro- The cat had normal vision in both eyes; vision was tizing pyogranulomatous reaction, with presence of diminished in the left eye showing limited response septate branching hyphae both regular and irregular, to the menace reflexe in this eyeball. The Schirmer morphologically compatible with Aspergillus sp. and I Tear Test (STT strips)1 was 16 mm/min in the right other hyaline septated mold (Figure 5). Special stai- eye and 3mm/min in the left eye. Intraocular pressure ning with Ziehl Nielsen techinique was performed for (IOP) was measured using applanation tonometry (To- mycobacteria investigation, but the result was negative. nopen® XL)2, after application of a topical ophthalmic The DNA was extracted from the formalin anesthetic solution (Anestalcon®)3. The IOP was 17 fixed paraffin embedded (FFPE) sample using the mmHg in the right eye and 48 mmHg in the left eye. QIAamp® FFPE tissue kit (Qiagen)5. DNA extracted 2
F.V.A. Costa, A. Spanamberg, R. Araujo, J. Werner & L. Ferreiro. 2019. Feline Sino-orbital Fungal Infection Caused by Aspergillus and Scopulariopsis. Acta Scientiae Veterinariae. 47(Suppl 1): 383. was detected with panfungal PCR using ITS3-F Ringer’s solution at the maintenance dose of 50 mL/ (5’-GCATCGATGAAGAACGCAGC-3’) and ITS4- kg/day. After 2 days of treatment, the animal died R (5’- TCCTCCGCTTATTGATATGC-3’ [34] for suddenly with a history of acute inspiratory dyspnea amplification of internal transcribed spacer 2 (ITS2) and cyanosis at the time prior to death. The animal’s region. PCR amplification was performed in a 25 μL owner declined to perform a necropsy. containing 1 μL of DNA extract, 12.5 μL Qiagen Taq DISCUSSION PCR master mix (Qiagen)5 and 0.5 μL of each primer (for a 0.2 μM final concentration of each primer). After Sino-orbital fungal disease is rare in cats and a preincubation at 94°C for 15 min, the amplification can result in significant injuries to the upper respira- was performed for a total of 35 cycles as follows: de- tory tract and eyes, sometimes resulting in enucleation naturation at 94°C for 30 s, annealing at 57°C for 90 and death. In this report, the patient was a Persian cat, s, extension at 72°C for 1 min, and a final extension agreeing with previous reports that 8 out of 12 cats step of 10 min at 72°C. The primers ITS3 and ITS4 treated for nasal or ocular aspergillosis were Persian amplify a fragment of between 300 and 400 bp. PCR or Himalayan [2,12,15,18,23,31,35]. It seems feasible product was separated on a 2% agarose. PCR product that a brachycephalic facial conformation may be an was purified using PuriLink® PCR Purification Kit important risk factor for the development of sino-nasal (Invitrogen)6, and sequencing to confirmed the pres- fungal disease in cats [29], because fungal organisms ence of fungal elements in the tissue sample. are a part of the normal feline ocular and nasal flora The sequencing analysis of the fragments re- [6,19] and it is possible that the brachycephalic airway vealed a clear mix of two fungal sequences (two peaks of Persian and Himalayan cats may at times become for each position). Aspergillus was initially cultured overwhelmed in its ability to clear Aspergillus spp. from the tissue, therefore the consensus profile for ITS2 from the cat’s upper airway [2]. Tomsa et al. [31] of 100 Aspergillus sequences was subtracted from the presupposed that susceptibility to localized fungal sequencing graph to obtain the sequence for the second infection can occur as a consequence of the possible fungus (e.g. for a sequencing position with A and C, if altered airflow observed in pronounced brachycephaly. the nucleotide of consensus Aspergillus sequence was This could cause changes in the vasomotor action of A, then the second position was considered to be C). the vasculature and decrease mucociliary clearance. At the end of this detailed analysis of each nucleotide Wilkinson et al. [36] reported two cats with sino-nasal position, two sequences were obtained. Basic local disease who also had involvement of the orbit. In one alignment search tool (BLAST®)7 was performed in case this was associated with fungal sinusitis. Our both sequences giving the results 100% match for As- patient had both presentations of this disease, with pergillus and Scopulariopsis respectively. No fungal the same clinical signs as reported for the sino-orbital species could be identified using these ITS2 sequences, (SOA) and SNA forms. The disease probably extended as these region was common (>99% match) to multiple beyond the sinonasal cavity and involved the adjacent species within each genus. orbital structure and palate. Therefore, the first presen- The patient was treated with intranasal clotrim- ting signs in cats are referable to orbital invasion [3]. azole once a week and systemic itraconazole at a dose In this case, the patient presented first orbital involve- of 50 mg orally per day. After 20 days of treatment, the ment, and the signs were exophthalmos, high intraocu- patient showed a mass of 2 cm in diameter on the left lar pressure, severe protrusion and inflammation of the side of the soft palate (Figure 6A), which was removed third eyelid. All of these signs were likely secondary surgically. However, recurrence occurred 7 days after to an invasive retrobulbar fungal granuloma that was surgery (Figure 6B), and the patient began to show pushing and compressing the eyeball, characterizing labored breathing due to obstruction of the oropharynx. the SOA form [2,3,15,35]. Furthermore, the patient Due to the rapid evolution of the disease and showed mucopurulent nasal and ocular discharge from poor response to treatment, the cat was treated with the same side, corroborating with Hamilton et al. [15] subcutaneous amphotericin B at 0.5 mg/kg diluted in and Barachetti et al. [2], which said that these signs 350 mL of warm 0.45% sodium chloride and 2.5% are commonly found in nasal aspergillosis. The corneal glucose, and intravenous fluid therapy with lactated and lacrimal film alterations, including the corneal 3
F.V.A. Costa, A. Spanamberg, R. Araujo, J. Werner & L. Ferreiro. 2019. Feline Sino-orbital Fungal Infection Caused by Aspergillus and Scopulariopsis. Acta Scientiae Veterinariae. 47(Suppl 1): 383. ulcer and low STT in the left eye, were possibly due to corneal exposure, a consequence of the exophthalmos and lagophthalmos [2,5,15,35]. Disseminated aspergillosis is apparently an opportunistic infection in immunosuppressed cats [26]. In contrast, incompetence of the immune system is not believed to be required for nasal infection. Only 2 of 16 previously reported cats with sinonasal or orbital aspergillosis had a confirmed immunosuppressive condition [12,15,18,23,31,35]. In this study, the animal had no history of trauma or previous infections and was negative for FIV and FeLV infection, both important causes of immunosuppression in cats. Figure 1. Patient showing protrusion, hyperemia, chemosis of the third eyelid and exophthalmos in the left eye. It’s possible to note nasal and Diagnostic imaging for orbital disease typically ocular mucopurulent discharge in the same side. includes skull radiography and orbital ultrasonography, however, CT and magnetic resonance imaging (MRI) have been successfully used to aid in the diagnosis of Figure 2. A- Lagophthalmos, corneal edema, neovascularization and mydriasis in the left eye. B- Visible corneal ulcer after the lesion retained fluo- rescein stain. Aspergillus spp. infections [15,16,25,29]. Radiography of the nasal cavity and frontal sinuses may show abnor- malities such as increased soft-tissue densities, loss of turbinates [9,16,31,35] and possible bone erosion/lysis [2,9], as the patient showed in this report. CT imaging is important for assessing the extent of the disease [35] because of its ability to generate cross-sectional images [8]. This technique is also useful to detect cal- cium accumulation within the fungus colony or bone destruction [25]. However, MRI is the best technique to diagnose soft tissue lesions and vascular invasion [16,25]. It can be used to evaluate more critically the optic chiasm, differentiate neoplasia and determine the full extent of the disease [2,25]. Occasionally, Figure 3. Inspection and biopsy of medial region of the left eye showing cytology of nasal discharge or nasal flush will show purulent and caseous tissue. septate hyphae. The presence of hyphae in the tissues 4
F.V.A. Costa, A. Spanamberg, R. Araujo, J. Werner & L. Ferreiro. 2019. Feline Sino-orbital Fungal Infection Caused by Aspergillus and Scopulariopsis. Acta Scientiae Veterinariae. 47(Suppl 1): 383. Figure 4. Left orbital cavity after the enucleation with purulent and case- Figure 5. Microscopy of sino-orbital lesion showing necrotic tissue with ous tissue. multiple irregular, septate branching hyphae, morphologically compatible with Aspergillus sp. and other hyaline septated mold [PAS; 200x]. Figure 6. After treatment with antifungal therapy. A- Mass of 2 cm in diameter in the soft palate on the left side. B- Recurrence of the lesion in the soft palate 7 days after surgery. will aid in differentiating diagnosis of Aspergillus spp. by septate hyaline hyphae (suggesting both regular from Mucor spp., and Candida spp. Infections [9]. and irregular structures), some with dichotomous However, sometimes it can be inconclusive [15,23], branching suggestive of Aspergillus sp. corroborating as in the case reported here. with previous reports [2,17,31,35]. Histopathology Occasionally, the results of fungal culture do has been used as the primary ante mortem diagnostic not distinguish between Aspergillus spp. colonization method of feline aspergillosis [10]. Biopsy samples and active infection [26]. False negatives can also occur are more likely to reveal the organisms, but false ne- [36]. Nevertheless, when a sample can be obtained gative biopsies occur if only the superficial aspect of directly from the site of visible fungal infection, a the lesion is biopsied [35]. positive fungal culture would provide useful adjunct Molecular methods are needed for correct fungal diagnostic information [23,31]. In this report, culture identification when the conventional methodologies from biopsied material revealed unique and abundant (histopathology and culture) does not allow the complete growth of Aspergillus spp. clarification. In our study, although the Aspergillus sp. In this case, histology showed inflammatory has grown in culture, PCR panfungal was required to proliferative necrotizing pyogranulomatous reaction, confirm fungal identification and a possible case of co- with the presence of severe fungal infection evidenced -presence of molds, due to histopathology suggesting 5
F.V.A. Costa, A. Spanamberg, R. Araujo, J. Werner & L. Ferreiro. 2019. Feline Sino-orbital Fungal Infection Caused by Aspergillus and Scopulariopsis. Acta Scientiae Veterinariae. 47(Suppl 1): 383. multiple fungi. The presence of another fungus, Sco- of clotrimazole is considered the treatment of choice pulariopsis, was confirmed by sequencing analysis of for canine nasal aspergillosis. The cure rate has been ITS2. In tissue the features of hyaline septated molds as high as 94%.28 This technique has been reported were similar to those seen with aspergillosis and Sco- effective in three cats with fungal rhinitis [12,31]. pulariopsis mycosis [13]. Two other cats were treated with a topical infusion of The most common causes of chronic nasal clotrimazole in previous reports [15,23]. One had no discharge in cats include nasal neoplasia, fungal response to treatment and the other responded initially sinorhinitis -Aspergillosis [6] and cryptococcosis but was euthanatized later because of the development [21,32] - upper respiratory complex [1,5,30,33] and of new clinical signs of dysphagia and anorexia. Both bacterial, allergic and idiopatic rhinitis [9]. The drugs of these cats had also SOA, similar to the case repor- available to treat fungal infections of the eyeball are ted here, while the cats that responded successfully to restricted because eyedrops have limited penetration clotrimazole had SNA. into the eyeball [11]. One option is topical itracona- In this case, the animal died suddenly. Cer- zole 1% which may be useful to treat corneal ulcers tainly, the brachycephalic conformation decreases caused by Aspergillus fumigatus [22]. In this case, only sinus aeration and drainage of respiratory secretions supportive therapy was prescribed until a definitive secondary to infection, polyps, and allergic rhinosi- diagnosis was made, that’s why a systemic treatment nusitis, which have been identified as risk factors for was preferably chosen. invasive SNA aspergillosis in human beings [3]. As Itraconazole generally has good in vitro activi- was observed, the patient had a mass in the soft palate, ty against Aspergillus spp., and itraconazole-resistant which was causing the difficulty to breath and feeding. strains are uncommonly seen [24].Azoles are by far This was probably the reason for death, because he the most ineffective agents, and amphotericin B has showed acute inspiratory dyspnea and cyanosis at his limited activity against Scopulariopsis spp. [27,28]. final hours. In this patient, oral itraconazole was initially selected Orbital aspergillosis/hialohyphomycosis is rare because of its documented efficacy against a variety of in cats and can result in significant injuries to the eyes, deep mycotic infections in cats and its relative safety sometimes resulting in enucleation. Nasal aspergillosis in this species [7]. But its effectiveness for treatment is also uncommon and can cause dyspnea and death of of aspergillosis has controversial results. Itraconazole cats through nasopharyngeal asphyxia. The association was effective in four cats with SNA aspergillosis, but of both forms can occur and, unfortunately, the treat- three of them had recurrence of clinical signs follo- ment is ineffective so far. Further studies are required wing discontinuation of treatment [31,35]. However, in order to better understand and efficiently treat fungal itraconazole was ineffective for a cat with orbital as- sino-orbital infections in this species. pergillosis [24]. In two studies of SOA, there was no clinical improvement with use of itraconazole and then MANUFACTURERS amphotericin B systemically [18,23]. Amphotericin B 1 Schering Plough Anima Health. Union, NJ, USA. has been used for more than 40 years in aspergillosis 2 Mentor O & O Inc. Norwell, MA, USA. 3 Allergan Pharmaceuticals. São Paulo, SP, Brazil. treatment and also targets the fungal cell membrane. 4 Ophthalmos Pharmaceuticals. São Paulo, SP, Brazil. Its less toxic lipid formulations have been used in 5 Qiagen. Hilden, Germany. cases of aspergillosis refractory to azole antifungals 6 Invitrogem. Carlsbad, CA, USA. [20]. Resistance to AMB is a rare phenomenon in A. 7 U.S. National Library of Medicine. Rockville, MD, USA. fumigatus, however A. terreus is intrinsically resistant Declaration of interest. The authors report no conflicts of and A. flavus has reduced sensitivity to this antifungal interest. The authors alone are responsible for the content and [14]. Topical therapy with a non-invasive infusion writing of paper. 6
F.V.A. Costa, A. Spanamberg, R. Araujo, J. Werner & L. Ferreiro. 2019. Feline Sino-orbital Fungal Infection Caused by Aspergillus and Scopulariopsis. Acta Scientiae Veterinariae. 47(Suppl 1): 383. REFERENCES 1 Andrew S.E. 2001. Ocular manifestations of feline herpesvirus. Journal Feline Medicine Surgery. 3: 9-16. 2 Barachetti L., Mortellaro C.M., Di Giancamillo M., Giudice C., Martino P., Travetti O. & Miller P.E. 2009. Bilateral orbital and nasal aspergillosis in a cat. Veterinary Ophthalmology. 12: 176-182. 3 Barrs V.R., Beatty J.A., Lingard A.E., Malik R., Krockenberger M.B., Martin P., O’Brien C., Angles J.M., Dowden M. & Halliday C. 2007. Feline sino-orbital aspergillosis: an emerging clinical syndrome. Australian Veteri- nary Journal. 85(3):23. 4 Barrs V.R. & Beatty J.A. 2010. Upper respiratory tract aspergillosis. In: August J.R. (Ed). Consultations in Feline Medicine. 6th edn. St. Louis: Saunders Elsevier, pp.36-52. 5 Barrs V.R. & Talbot J.J. 2014. Feline aspergillosis. The Veterinary Clinics of North America Small Animal Practice. 44(1): 51-73 6 Benitah N. 2006. Canine Nasal Aspergillosis. Clinical Techniques Small Animal Practice. 21: 82-88. 7 Boothe D.M., Herring I., Calvin J., Way N. & Dvorak J. 1997. Itraconazole disposition after single oral and intra- venous and multiple oral dosing in healthy cats. America Journal Veterinary Research.58: 872-877. 8 Choi M.Y., Bae I.H., Lee J.H. & Lee S.J. 2002. Aspergillosis presenting as an optic neuritis. Korean Journal of Ophthalmology.16: 119-123. 9 Codner E.C., Lurus A.G., Miller J.B., Gavin P.R., Gallina A. & Barbee D.D. 1993. Comparison of computed tomography with radiography as a noninvasive diagnostic technique for chronic nasal disease in dogs. Journal of the American Veterinary Medical Association. 202: 1106-1110. 10 Davies C. & Troy G. 1996. Deep mycotic infections in cats. Journal of the American Veterinary Medical Association. 32: 380-391. 11 Freda R. 2006. Use of oral voriconazole as adjunctive treatment of severe cornea fungal infection: case report. Arquivos Brasileiros de Oftalmologia. 69: 431-434. 12 Furrow E. & Groman R.P. 2009. Intranasal infusion of clotrimazole for the treatment of nasal aspergillosis in two cats. Journal of the American Veterinary Medical Association. 235: 1188-1193. 13 Guarner J. & Brandt M.E. 2011. Histopathologic diagnosis of fungal infections in the 21st century - Clinical micro- biology reviews. Journal of the American Veterinary Medical Association. 213: 501-506. 14 Gonçalves S.S., Souza A.C.R., Chowdhary A., Meis J.F. & Colombo A.L. 2016. Epidemiology and molecular mechanisms of antifungal resistance in Candida and Aspergillus. Mycoses. 59: 198-219. 15 Hamilton H.L., Whitley R.D. & McLaughlin S.A. 2000. Exophthalmos secondary to aspergillosis in a cat. Journal of the American Animal Hospital Association. 36: 343-347. 16 Hartmann K., Lloret A., Pennisi M.G., Ferrer L., Addie D., Belák S., Boucraut-Baralon C., Egberink H., Frymus T., Gruffydd-Jones T., Hosie M.J., Lutz H., Marsilio F., Möstl K., Radford A.D., Thiry E., Truyen U. & Horzinek M.C. 2013. Aspergillosis in cats: ABCD guidelines on prevention and management. Journal of Feline Medicine and Surgery. 15(7): 605-610. 17 Hazell K.L.A., Swift I.M. & Sullivan N. 2011. Successful treatment of pulmonary aspergillosis in a cat. Australian Veterinary Journal. 89(3): 101-104. 18 Kano R., Itamoto K., Okuda M., Inokuma H., Hasegawa A. & Balajee S.A. 2008. Isolation of Aspergillus udagawae from a fatal case of feline orbital aspergillosis. Mycoses. 51: 360-361. 19 Labelle A.L., Hamor R.E., Barger Anne M., Maddox C.W. & Breaux C.B. 2009. Aspergillus flavus keratomycosis in a cat treated with topical 1% voriconazole solution. Veterinary Ophthalmology. 12: 48-52. 20 Linden P.K. 2003. Amphotericin B lipid complex for treatment of invasive fungal infections. Expert Opinion on Pharmacotherapy. 4: 2099-2110. 21 Malik R., Wigney D.I., Muir D.B. & Love D.N. 1997. Asymptomatic carriage of Cryptococcus neoformans in the nasal cavity of dogs and cats. Journal of Medical and Veterinary Mycology. 35: 27-31. 22 Martínez-Ramos M., Claros-B J.A., Vale-Oviedo M.A., Siso-Villarroel E., Padilla R., Santiago A. & Simón J.A. 2008. Effect of the vehicle on the topical itraconazole efficacy for treating corneal ulcers caused by Aspergillus fumigatus. Clinical and Experimental Ophthalmology. 36: 335-338. 23 McLellan G.J., Aquino S.M., Mason D.R., Kinyon J.M. & Myers R.K. 2006. Use of posaconazole in the manage- ment of invasive orbital aspergillosis in a cat. Journal of the American Animal Hospital Association. 42: 302-307. 7
F.V.A. Costa, A. Spanamberg, R. Araujo, J. Werner & L. Ferreiro. 2019. Feline Sino-orbital Fungal Infection Caused by Aspergillus and Scopulariopsis. Acta Scientiae Veterinariae. 47(Suppl 1): 383. 24 Moore C.B., Sayers N., Mosquera J., Slaven J. & Denning D.W. 2000. Antifungal drug resistance in Aspergillus. Journal of Infection. 41: 203-220. 25 Morgan R.V. 2011. Aspergillosis, Nasal (Zoonotic). Available at: www.vin.com/Members/Associate/Associate. plx?DiseaseId=2088. [Accessed online in February 2011]. 26 Sharp N.J.H. 1998. Canine nasal aspergillosis-penicilliosis. In: Greene C.E. (Ed). Infectious diseases of the dog and cat. 2nd edn. Philadelphia: WB Saunders Co, pp.404-409. 27 Skóra M., Bulanda M. & Jagielski T. 2015. In vitro activities of a wide panel of antifungal drugs against various Scopulariopsis and Microascus species. Antimicrobial Agents and Chemotherapy. 59(9): 5827-5829. 28 Skóra M., Macura A.B. & Bulanda M. 2014. In vitro antifungal susceptibility of Scopulariopsis brevicaulis isolates. Medical Mycology. 52(7): 723-727. 29 Sykes J.E. 2014. Canine and Feline Infectious Diseases. St. Louis: Elsevier Saunders, 915p. 30 Thiry E., Addie D., Belák S., Boucraut-Baralon C., Egberink H., Frymus T., Gruffydd-Jones T., Hartmann K., Hosie M.J., Lloret A., Lutz H., Marsilio F., Pennisi M.G., Radford A.D., Truyen U. & Horzinek M.C. 2009. Feline herpesvirus infection. ABCD guidelines on prevention and management. Journal Feline Medicine Surgery. 11: 547-555. 31 Tomsa K., Glaus T.M., Zimmer C. & Greene C.E. 2003. Fungal rhinitis and sinusitis in three cats. Journal of the American Veterinary Medical Association. 222: 1380-1384. 32 Trivedi S.R., Sykes J.E., Cannon M.S., Wisner E.R., Meyer W., Sturges B.K., Dickinson P.J. & Johnson L.R. 2011. Clinical features and epidemiology of cryptococcosis in cats and dogs in California: 93 cases (1988-2010). Journal of the American Veterinary Medical Association. 239: 357-369. 33 Volopich S., Benetka V., Schwendenwein I., Möstl K., Sommerfeld-Stur I. & Nell B. 2005. Cytologic findings, and feline herpesvirus DNA and Chlamydophila felis antigen detection rates in normal cats and cats with conjunctival and corneal lesions. Veterinary Ophthalmology. 8: 25-32. 34 White T.J., Bruns T., Lee S. & Taylor J. 1990. Amplication and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M.A., Gelfand D.H., Sninsky J.J. & White T.J. (Eds). PCR protocols: a guide to methods and applications. San Diego: Academic Press Inc., pp.315-322. 35 Whitney B.L., Broussard J. & Stefanacci J.D. 2005. Four cats with fungal rhinitis. Journal Feline Medicine Surgery. 7: 53-58. 36 Wilkinson G.T., Sutton R.H. & Grono L.R. 1982. Aspergillus spp. infection associated with orbital cellulitis and sinusitis in a cat. Journal of Small Animal Practice. 23: 127-131. CR383 http://seer.ufrgs.br/ActaScientiaeVeterinariae 8
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